Rapid X-ray photoreduction of dimetal-oxygen cofactors in ribonucleotide reductase

Journal of Biological Chemistry

Volumn 288, Issue 14, 2013, Pages 9648-9661

  Sigfridsson, Kajsa G V ^b   Chernev, Petko ^b   Leidel, Nils ^b   Popović Bijelić, Ana ^a,c   Gräslund, Astrid ^a   Haumann, Michael ^b  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

[No Author keywords available]

Indexed keywords

CHLAMYDIA TRACHOMATIS; CRYOGENIC TEMPERATURES; DENSITY FUNCTIONAL THEORY CALCULATIONS; METAL COORDINATION; METAL-METAL DISTANCES; PROTEIN CRYSTALLOGRAPHY; RIBONUCLEOTIDE REDUCTASE; X-RAY PHOTOREDUCTION;

CHEMICAL ACTIVATION; DENSITY FUNCTIONAL THEORY; MANGANESE; MINERALOGY; MODEL STRUCTURES; PROTEINS; REDOX REACTIONS; X RAY ABSORPTION SPECTROSCOPY;

CRYSTALLOGRAPHY;

IRON; MANGANESE DERIVATIVE; MEMBRANE COFACTOR PROTEIN; RIBONUCLEOTIDE REDUCTASE;

ARTICLE; BINDING SITE; CATALYSIS; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DENSITY FUNCTIONAL THEORY; ENZYME KINETICS; LIMIT OF DETECTION; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN STRUCTURE; ROOM TEMPERATURE; X RAY ABSORPTION SPECTROSCOPY;

AMINO ACID MOTIFS; CHLAMYDIA TRACHOMATIS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; IONS; IRON; KINETICS; LIGHT; MANGANESE; METALS; MODELS, CHEMICAL; OXYGEN; PHOTOCHEMISTRY; RECOMBINANT PROTEINS; RIBONUCLEOTIDE REDUCTASES; TEMPERATURE; X-RAYS;

CHLAMYDIA TRACHOMATIS;

EID: 84875993794     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.438796     Document Type: Article

References (115)

1. Cotruvo, J. A., and Stubbe, J. (2011) Class I ribonucleotide reductases. Metallocofactor assembly and repair in vitro and in vivo. Annu. Rev. Biochem. 80, 733-767
2. Nordlund, P., and Reichard, P. (2006) Ribonucleotide reductases. Annu. Rev. Biochem. 75, 681-706
3. Sjöberg, B. M., and Gräslund, A. (1983) Ribonucleotide reductase. Adv. Inorg. Biochem. 5, 87-110
4. Tinberg, C. E., and Lippard, S. J. (2011) Dioxygen activation in soluble methane monooxygenase. Acc. Chem. Res. 44, 280-288
5. Westerheide, L., Pascaly, M., and Krebs, B. (2000) Methane monooxygenase and its related biomimetic models. Curr. Opin. Chem. Biol. 4, 235-241
6. Lange, S. J., and Que, L., Jr. (1998) Oxygen activating nonheme iron enzymes. Curr. Opin. Chem. Biol. 2, 159-172
7. Högbom, M. (2010) The manganese/iron-carboxylate proteins. What is what, where are they, and what can the sequences tell us? J. Biol. Inorg. Chem. 15, 339-349
8. Krebs, C., Matthews, M. L., Jiang, W., and Bollinger, J. M., Jr. (2007) AurF from Streptomyces thioluteus and a possible new family of manganese/iron oxygenases. Biochemistry 46, 10413-10418
9. Herrick, J., and Sclavi, B. (2007) Ribonucleotide reductase and the regulation of DNA replication. An old story and an ancient heritage. Mol. Microbiol. 63, 22-34
10. Brignole, E. J., Ando, N., Zimanyi, C. M., and Drennan, C. L. (2012) The prototypic class Ia ribonucleotide reductase from Escherichia coli. Still surprising after all these years. Biochem. Soc. Trans. 40, 523-530
11. Kolberg, M., Strand, K. R., Graff, P., and Andersson, K. K. (2004) Structure, function, and mechanism of ribonucleotide reductases. Biochim. Biophys. Acta 1699, 1-34
12. Bollinger, J. M., Jr., and Krebs, C. (2006) Stalking intermediates in oxygen activation by iron enzymes. Motivation and method. J. Inorg. Biochem. 100, 586-605
13. Que, L., Jr. (1991) Oxygen activation at the diiron center of ribonucleotide reductase. Science 253, 273-274
14. Que, L., Jr. (2004) The oxo/peroxo debate. A nonheme iron perspective. J. Biol. Inorg. Chem. 9, 684-690
15. Han, W. G., Liu, T., Lovell, T., and Noodleman, L. (2006) Seven clues to the origin and structure of class-I ribonucleotide reductase intermediate X. J. Inorg. Biochem. 100, 771-779
16. Mitić, N., Clay, M. D., Saleh, L., Bollinger, J. M., Jr., and Solomon, E. I. (2007) Spectroscopic and electronic structure studies of intermediate X in ribonucleotide reductase R2 and two variants. A description of the FeIV-oxo bond in the FeIII-O-FeIV dimer. J. Am. Chem. Soc. 129, 9049-9065
17. Burdi, D. W., Willems, J. P., Riggs-Gelasco, P., Antholine, W. E., Stubbe, J., and Hoffman, B. M. (1998) The core structure of X generated in the assembly of the di-iron cluster of ribonucleotide reductase. 17O2 and H217O ENDOR. J. Am. Chem. Soc. 120, 12910-12919
18. Reece, S. Y., Hodgkiss, J. M., Stubbe, J., and Nocera, D. G. (2006) Protoncoupled electron transfer. The mechanistic underpinning for radical transport and catalysis in biology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1351-1364
19. Adrait, A., Ohrström, M., Barra, A. L., Thelander, L., and Gräslund, A. (2002) EPR studies on a stable sulfinyl radical observed in the iron-oxygen-reconstituted Y177F/I263C protein R2 double mutant of ribonucleotide reductase from mouse. Biochemistry 41, 6510-6516
20. Licht, S., Gerfen, G. J., and Stubbe, J. (1996) Thiyl radicals in ribonucleotide reductases. Science 271, 477-481
21. Mao, S. S., Holler, T. P., Yu, G. X., Bollinger, J. M., Jr., Booker, S., Johnston, M. I., and Stubbe, J. (1992) A model for the role of multiple cysteine residues involved in ribonucleotide reduction. Amazing and still confusing. Biochemistry 31, 9733-9743
22. Prinz, W. A., Aslund, F., Holmgren, A., and Beckwith, J. (1997) The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm. J. Biol. Chem. 272, 15661-15667
23. Stubbe, J., and Riggs-Gelasco, P. (1998) Harnessing free radicals. Formation and function of the tyrosyl radical in ribonucleotide reductase. Trends Biochem. Sci. 23, 438-443
24. Högbom, M., Stenmark, P., Voevodskaya, N., McClarty, G., Gräslund, A., and Nordlund, P. (2004) The radical site in chlamydial ribonucleotide reductase defines a new R2 subclass. Science 305, 245-248
25. Voevodskaya, N., Lendzian, F., Ehrenberg, A., and Gräslund, A. (2007) High catalytic activity achieved with a mixed manganese-iron site in protein R2 of Chlamydia ribonucleotide reductase. FEBS Lett. 581, 3351-3355
26. Boal, A. K., Cotruvo, J. A., Jr., Stubbe, J., and Rosenzweig, A. C. (2010) Structural basis for activation of class Ib ribonucleotide reductase. Science 329, 1526-1530
27. Jiang, W., Yun, D., Saleh, L., Barr, E. W., Xing, G., Hoffart, L. M., Maslak, M. A., Krebs, C., and Bollinger, J. M., Jr. (2007) A manganese(IV)/iron (III) cofactor in Chlamydia trachomatis ribonucleotide reductase. Science 316, 1188-1191
28. Bollinger, J. M., Jr., Jiang, W., Green, M. T., and Krebs, C. (2008) The manganese(IV)/iron(III) cofactor of Chlamydia trachomatis ribonucleotide reductase. Structure, assembly, radical initiation, and evolution. Curr. Opin. Struct. Biol. 18, 650-657
29. Voevodskaya, N., Lendzian, F., Sanganas, O., Grundmeier, A., Gräslund, A., and Haumann, M. (2009) Redox intermediates of the Mn-Fe site in subunit R2 of Chlamydia trachomatis ribonucleotide reductase. An xray absorption and EPR study. J. Biol. Chem. 284, 4555-4566
30. Leidel, N., Popović-Bijelić, A., Havelius, K. G., Chernev, P., Voevodskaya, N., Gräslund, A., and Haumann, M. (2012) High-valent [MnFe] and [FeFe] cofactors in ribonucleotide reductases. Biochim. Biophys. Acta 1817, 430-444
31. Voevodskaya, N., Lendzian, F., and Gräslund, A. (2005) A stable FeIIIFeIV replacement of tyrosyl radical in a class I ribonucleotide reductase. Biochem. Biophys. Res. Commun. 330, 1213-1216
32. Voevodskaya, N., Galander, M., Högbom, M., Stenmark, P., McClarty, G., Gräslund, A., and Lendzian, F. (2007) Structure of the high-valent FeIIIFeIV state in ribonucleotide reductase (RNR) of Chlamydia trachomatis. Combined EPR, 57Fe-, 1H-ENDOR and x-ray studies. Biochim. Biophys. Acta 1774, 1254-1263
33. Schenk, G., Boutchard, C. L., Carrington, L. E., Noble, C. J., Moubaraki, B., Murray, K. S., de Jersey, J., Hanson, G. R., and Hamilton, S. (2001) A purple acid phosphatase from sweet potato contains an antiferromagnetically coupled binuclear Fe-Mn center. J. Biol. Chem. 276, 19084-19088
34. Andersson, C. S., and Högbom, M. (2009) A Mycobacterium tuberculosis ligand-binding Mn/Fe protein reveals a new cofactor in a remodeled R2-protein scaffold. Proc. Natl. Acad. Sci. U.S.A. 106, 5633-5638
35. Högbom, M. (2011) Metal use in ribonucleotide reductase R2, di-iron, di-manganese and heterodinuclear. An intricate bioinorganic workaround to use different metals for the same reaction. Metallomics 3, 110-120
36. Cotruvo, J. A., Jr., and Stubbe, J. (2012) Metallation and mismetallation of iron and manganese proteins in vitro and in vivo. The class I ribonucleotide reductases as a case study. Metallomics 4, 1020-1036
37. Boal, A. K., Cotruvo, J. A., Jr., Stubbe, J., and Rosenzweig, A. C. (2012) The dimanganese(II) site of Bacillus subtilis class Ib ribonucleotide reductase. Biochemistry 51, 3861-3871
38. Cotruvo, J. A., Jr., and Stubbe, J. (2010) An active dimanganese(III)- tyrosyl radical cofactor in Escherichia coli class Ib ribonucleotide reductase. Biochemistry 49, 1297-1309
39. Cox, N., Ogata, H., Stolle, P., Reijerse, E., Auling, G., and Lubitz, W. (2010) A tyrosyl-dimanganese coupled spin system is the native metalloradical cofactor of the R2F subunit of the ribonucleotide reductase of Corynebacterium ammoniagenes. J. Am. Chem. Soc. 132, 11197-11213
40. Lambertz, C., Leidel, N., Havelius, K. G., Noth, J., Chernev, P., Winkler, M., Happe, T., and Haumann, M. (2011) O2 reactions at the six-iron active site (H-cluster) in [FeFe]-hydrogenase. J. Biol. Chem. 286, 40614-40623
41. Andersson, C. S.,Öhrström, M., Popović-Bijelić, A., Gräslund, A., Stenmark, P., and Högbom, M. (2012) The manganese ion of the heterodinuclear Mn/Fe cofactor in Chlamydia trachomatis ribonucleotide reductase R2c is located at metal position 1. J. Am. Chem. Soc. 134, 123-125
42. Dassama, L. M., Boal, A. K., Krebs, C., Rosenzweig, A. C., and Bollinger, J. M., Jr. (2012) Evidence that the beta subunit of Chlamydia trachomatis ribonucleotide reductase is active with the manganese ion of its manganese (IV)/iron(III) cofactor in site 1. J. Am. Chem. Soc. 134, 2520-2523
43. Que, L., Jr., and Tolman, W. B. (2002) Bis(mu-oxo)dimetal "diamond" cores in copper and iron complexes relevant to biocatalysis. Angew. Chem. Int. Ed. Engl. 41, 1114-1137
44. Roos, K., and Siegbahn, P. E. (2011) Oxygen cleavage with manganese and iron in ribonucleotide reductase from Chlamydia trachomatis. J. Biol. Inorg. Chem. 16, 553-565
45. Griese, J. J., and Högbom, M. (2012) X-ray reduction correlates with soaking accessibility as judged from four non-crystallographically related diiron sites. Metallomics 4, 894-898
46. Garman, E. F. (2010) Radiation damage in macromolecular crystallography. What is it and why should we care? Acta Crystallogr. D Biol. Crystallogr. 66, 339-351
47. Holton, J. M. (2009) A beginner's guide to radiation damage. J. Synchrotron Radiat. 16, 133-142
48. Sommerhalter, M., Lieberman, R. L., and Rosenzweig, A. C. (2005) X-ray crystallography and biological metal centers. Is seeing believing? Inorg. Chem. 44, 770-778
49. Högbom, M., Huque, Y., Sjöberg, B. M., and Nordlund, P. (2002) Crystal structure of the di-iron/radical protein of ribonucleotide reductase from Corynebacterium ammoniagenes. Biochemistry 41, 1381-1389
50. Lindqvist, Y., Huang, W., Schneider, G., and Shanklin, J. (1996) Crystal structure of (9) stearoyl-acyl carrier protein desaturase from castor seed and its relationship to other di-iron proteins. EMBO J. 15, 4081-4092
51. Logan, D. T., Su, X. D., Aberg, A., Regnström, K., Hajdu, J., Eklund, H., and Nordlund, P. (1996) Crystal structure of reduced protein R2 of ribonucleotide reductase. The structural basis for oxygen activation at a dinuclear iron site. Structure 4, 1053-1064
52. Schlichting, I., Berendzen, J., Chu, K., Stock, A. M., Maves, S. A., Benson, D. E., Sweet, R. M., Ringe, D., Petsko, G. A., and Sligar, S. G. (2000) The catalytic pathway of cytochrome P450cam at atomic resolution. Science 287, 1615-1622
53. Berglund, G. I., Carlsson, G. H., Smith, A. T., Szöke, H., Henriksen, A., and Hajdu, J. (2002) The catalytic pathway of horseradish peroxidase at high resolution. Nature 417, 463-468
54. Adam, V., Royant, A., Nivière, V., Molina-Heredia, F. P., and Bourgeois, D. (2004) Structure of superoxide reductase bound to ferrocyanide and active site expansion upon x-ray-induced photoreduction. Structure 12, 1729-1740
55. Wuerges, J., Lee, J. W., Yim, Y. I., Yim, H. S., Kang, S. O., and Djinovic Carugo, K. (2004) Crystal structure of nickel-containing superoxide dismutase reveals another type of active site. Proc. Natl. Acad. Sci. U.S.A. 101, 8569-8574
56. Kühnel, K., Jarchau, T., Wolf, E., Schlichting, I., Walter, U., Wittinghofer, A., and Strelkov, S. V. (2004) The VASP tetramerization domain is a right-handed coiled coil based on a 15-residue repeat. Proc. Natl. Acad. Sci. U.S.A. 101, 17027-17032
57. Hough, M. A., Antonyuk, S. V., Strange, R. W., Eady, R. R., and Hasnain, S. S. (2008) Crystallography with online optical and x-ray absorption spectroscopies demonstrates an ordered mechanism in copper nitrite reductase. J. Mol. Biol. 378, 353-361
58. Yano, J., Kern, J., Irrgang, K. D., Latimer, M. J., Bergmann, U., Glatzel, P., Pushkar, Y., Biesiadka, J., Loll, B., Sauer, K., Messinger, J., Zouni, A., and Yachandra, V. K. (2005) X-ray damage to the Mn4Ca complex in single crystals of photosystem II. A case study for metalloprotein crystallography. Proc. Natl. Acad. Sci. U.S.A. 102, 12047-12052
59. Haumann, M., Liebisch, P., Müller, C., Barra, M., Grabolle, M., and Dau, H. (2005) Photosynthetic O2 formation tracked by time-resolved x-ray experiments. Science 310, 1019-1021
60. Grabolle, M., Haumann, M., Müller, C., Liebisch, P., and Dau, H. (2006) Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by x-ray irradiation at 10-300 K. J. Biol. Chem. 281, 4580-4588
61. Yi, J., Orville, A. M., Skinner, J. M., Skinner, M. J., and Richter-Addo, G. B. (2010) Synchrotron X-ray-induced photoreduction of ferric myoglobin nitrite crystals gives the ferrous derivative with retention of the O-bonded nitrite ligand. Biochemistry 49, 5969-5971
62. Purwar, N., McGarry, J. M., Kostera, J., Pacheco, A. A., and Schmidt, M. (2011) Interaction of nitric oxide with catalase. Structural and kinetic analysis. Biochemistry 50, 4491-4503
63. Dau, H., and Haumann, M. (2008) The manganese complex of photosystem II in its reaction cycle. Basic framework and possible realization at the atomic level. Coord. Chem. Rev. 252, 273-295
64. Cotelesage, J. J., Pushie, M. J., Grochulski, P., Pickering, I. J., and George, G. N. (2012) Metalloprotein active site structure determination. Synergy between X-ray absorption spectroscopy and X-ray crystallography. J. Inorg. Biochem. 115, 127-137
65. Shi, W., and Chance, M. R. (2011) Metalloproteomics. Forward and reverse approaches in metalloprotein structural and functional characterization. Curr. Opin. Chem. Biol. 15, 144-148
66. Younker, J. M., Krest, C. M., Jiang, W., Krebs, C., Bollinger, J. M., Jr., and Green, M. T. (2008) Structural analysis of the Mn(IV)/Fe(III) cofactor of Chlamydia trachomatis ribonucleotide reductase by extended x-ray absorption fine structure spectroscopy and density functional theory calculations. J. Am. Chem. Soc. 130, 15022-15027
67. Riggs-Gelasco, P. J., Shu, L. J., Chen, S. X., Burdi, D., Huynh, B. H., Que, L., and Stubbe, J. (1998) EXAFS characterization of the intermediate X generated during the assembly of the Escherichia coli ribonucleotide reductase R2 diferric tyrosyl radical cofactor. J. Am. Chem. Soc. 120, 849-860
68. Baldwin, J., Krebs, C., Saleh, L., Stelling, M., Huynh, B. H., Bollinger, J. M., Jr., and Riggs-Gelasco, P. (2003) Structural characterization of the peroxodiiron(III) intermediate generated during oxygen activation by the W48A/D84E variant of ribonucleotide reductase protein R2 from Escherichia coli. Biochemistry 42, 13269-13279
69. Petrie, S., Gatt, P., Stranger, R., and Pace, R. J. (2012) Modelling the metal atom positions of the photosystem II water oxidising complex. A density functional theory appraisal of the 1.9-Å resolution crystal structure. Phys. Chem. Chem. Phys. 14, 11333-11343
70. Grundmeier, A., and Dau, H. (2012) Structural models of the manganese complex of photosystem II and mechanistic implications. Biochim. Biophys. Acta 1817, 88-105
71. Popović-Bijelić, A., Voevodskaya, N., Domkin, V., Thelander, L., and Gräslund, A. (2009) Metal binding and activity of ribonucleotide reductase protein R2 mutants. Conditions for formation of the mixed manganese-iron cofactor. Biochemistry 48, 6532-6539
72. Klockenkämper, R. (1996) Total Reflection X-ray Fluorescence Analysis, Wiley-VCH, London, UK
73. Stripp, S., Sanganas, O., Happe, T., and Haumann, M. (2009) The structure of the active site H-cluster of [FeFe] hydrogenase from the green alga Chlamydomonas reinhardtii studied by x-ray absorption spectroscopy. Biochemistry 48, 5042-5049
74. Haumann, M.,Müller, C., Liebisch, P., Iuzzolino, L., Dittmer, J., Grabolle, M., Neisius, T., Meyer-Klaucke, W., and Dau, H. (2005) Structural and oxidation state changes of the photosystem II manganese complex in four transitions of the water oxidation cycle (S03S1, S13S2, S23S3, and S3,4 3S0) characterized by x-ray absorption spectroscopy at 20 K and room temperature. Biochemistry 44, 1894-1908
75. Dau, H., Liebisch, P., and Haumann, M. (2003) X-ray absorption spectroscopy to analyze nuclear geometry and electronic structure of biological metal centers. Potential and questions examined with special focus on the tetra-nuclear manganese complex of oxygenic photosynthesis. Anal. Bioanal. Chem. 376, 562-583
76. Zabinsky, S. I., Rehr, J. J., Ankudinov, A. L., Albers, R. C., and Eller, M. J. (1995) Multiple-scattering calculations of x-ray absorption spectra. Phys. Rev. B 52, 2995-3009
77. Rehr, J. J. (2006) Theory and calculations of X-ray spectra. XAS, XES, XRS, and NRIXS. Radiat. Phys. Chem. 75, 1547-1558
78. Liu, W. T., and Thorp, H. H. (1993) Bond valence sum analysis of metalligand bond lengths in metalloenzymes and model complexes. 2. Refined distances and other enzymes. Inorg. Chem. 32, 4102-4105
79. Neese, F. (2008) ORCA. An ab initio, DFT, and semiempirical electronic structure package version 2.6.35. Theoretical Chemistry Group, Max-Planck Institute for Chemical Energy Conversion, Mühlheim, Germany
80. Chernev, P., Zaharieva, I., Dau, H., and Haumann, M. (2011) Carboxylate shifts steer interquinone electron transfer in photosynthesis. J. Biol. Chem. 286, 5368-5374
81. Becke, A. D. (1988) Density-functional exchange-energy approximation with correct asymptotic behavior. Phys. Rev. A 38, 3098-3100
82. Schäfer, A., Huber, C., and Ahlrichs, R. (1994) Fully optimized contracted Gaussian basis sets of triple ζ valence quality for atoms Li to Kr. J. Chem. Phys. 100, 5829-5835
83. Weigend, F. (2006) Accurate Coulomb-fitting basis sets for H to Rn. Phys. Chem. Chem. Phys. 8, 1057-1065
84. Sinnecker, S., Rajendran, A., Klamt, A., Diedenhofen, M., and Neese, F. (2006) Calculation of solvent shifts on electronic g-tensors with the conductor-like screening model (COSMO) and its self-consistent generalization to real solvents (Direct COSMO-RS). J. Phys. Chem. A 110, 2235-2245
85. Seal, P., and Chakrabarti, S. (2008) Magnetic interactions in alkyl substituted cyclohexane diradical systems. A broken symmetry approach. J. Phys. Chem. A 112, 3409-3413
86. Sinnecker, S., Neese, F., Noodleman, L., and Lubitz, W. (2004) Calculating the electron paramagnetic resonance parameters of exchange coupled transition metal complexes using broken symmetry density functional theory. Application to a Mn-III/Mn-IV model compound. J. Am. Chem. Soc. 126, 2613-2622
87. Zwart, P. H., and Lamzin, V. S. (2003) Distance distributions and electron density characteristics of protein models. Acta Crystallogr. D Biol. Crystallogr. 59, 2104-2113
88. Westre, T. E., Kennepohl, P., DeWitt, J. G., Hedman, B., Hodgson, K. O., and Solomon, E. I. (1997) A multiplet analysis of Fe K-edge 1s 3 3d pre-edge features of iron complexes. J. Am. Chem. Soc. 119, 6297-6314
89. Visser, H., Anxolabéhère-Mallart, E., Bergmann, U., Glatzel, P., Robblee, J. H., Cramer, S. P., Girerd, J. J., Sauer, K., Klein, M. P., and Yachandra, V. K. (2001) Mn K-edge XANES and K, XES studies of two Mn-oxo binuclear complexes. Investigation of three different oxidation states relevant to the oxygen-evolving complex of photosystem II. J. Am. Chem. Soc. 123, 7031-7039
90. Roos, K., and Siegbahn, P. E. (2009) Density functional theory study of the manganese-containing ribonucleotide reductase from Chlamydia trachomatis. Why manganese is needed in the active complex. Biochemistry 48, 1878-1887
91. Han, W. G., Giammona, D. A., Bashford, D., and Noodleman, L. (2010) Density functional theory analysis of structure, energetics, and spectroscopy for the Mn-Fe active site of Chlamydia trachomatis ribonucleotide reductase in four oxidation states. Inorg. Chem. 49, 7266-7281
92. Beitlich, T., Kühnel, K., Schulze-Briese, C., Shoeman, R. L., and Schlichting, I. (2007) Cryoradiolytic reduction of crystalline heme proteins. Analysis by UV-Vis spectroscopy and x-ray crystallography. J. Synchrotron Radiat. 14, 11-23
93. Dubois, L., Jacquamet, L., Pecaut, J., and Latour, J. M. (2006) X-ray photoreduction of a di(mu-oxo)Mn(III)Mn(IV) complex occurs at temperatures as low as 20 K. Chem. Commun. (Camb.) 43, 4521-4523
94. de Serrano, V. S., Davis, M. F., Gaff, J. F., Zhang, Q., Chen, Z., D'Antonio, E. L., Bowden, E. F., Rose, R., and Franzen, S. (2010) X-ray structure of the metcyano form of dehaloperoxidase from Amphitrite ornata. Evidence for photoreductive dissociation of the iron-cyanide bond. Acta Crystallogr. D Biol. Crystallogr. 66, 770-782
95. Kim, J. H., Kim, Y. K., and Kang, H. (2009) Proton transfer and H/D isotopic exchange of water molecules mediated by hydroxide ions on ice film surfaces. J. Chem. Phys. 131, 044705
96. Chen, S. H. and Loong, C. K. (2006) Neutron scattering investigations of proton dynamics of water and hydroxyl species in confined geometries. Nuclear Engineer. Technol. 38, 201-224
97. Rasaiah, J. C., Garde, S., and Hummer, G. (2008) Water in nonpolar confinement. From nanotubes to proteins and beyond. Annu. Rev. Phys. Chem. 59, 713-740
98. Hermes, S., Bremm, O., Garczarek, F., Derrien, V., Liebisch, P., Loja, P., Sebban, P., Gerwert, K., and Haumann, M. (2006) A time-resolved ironspecific X-ray absorption experiment yields no evidence for an Fe2+ → Fe3+ transition during QA→QB electron transfer in the photosynthetic reaction center. Biochemistry 45, 353-359
99. Högbom, M., Galander, M., Andersson, M., Kolberg, M., Hofbauer, W., Lassmann, G., Nordlund, P., and Lendzian, F. (2003) Displacement of the tyrosyl radical cofactor in ribonucleotide reductase obtained by singlecrystal high-field EPR and 1.4-Å x-ray data. Proc. Natl. Acad. Sci. U.S.A. 100, 3209-3214
100. Voegtli, W. C., Sommerhalter, M., Saleh, L., Baldwin, J., Bollinger, J. M., Jr., and Rosenzweig, A. C. (2003) Variable coordination geometries at the diiron(II) active site of ribonucleotide reductase R2. J. Am. Chem. Soc. 125, 15822-15830
101. Leidel, N., Chernev, P., Havelius, K. G., Schwartz, L., Ott, S., and Haumann, M. (2012) Electronic structure of an [FeFe] hydrogenase model complex in solution revealed by x-ray absorption spectroscopy using narrow-band emission detection. J. Am. Chem. Soc. 134, 14142-14157
102. Dau, H., and Zaharieva, I. (2009) Principles, efficiency, and blueprint character of solar-energy conversion in photosynthetic water oxidation. Acc. Chem. Res. 42, 1861-1870
103. Vass, I., and Styring, S. (1991) pH-Dependent charge equilibria between tyrosine-D and the S states in photosystem II. Estimation of relative midpoint redox potentials. Biochemistry 30, 830-839
104. Magnuson, A., Liebisch, P., Högblom, J., Anderlund, M. F., Lomoth, R., Meyer-Klaucke, W., Haumann, M., and Dau, H. (2006) Bridging-type changes facilitate successive oxidation steps at about 1 V in twobinuclear manganese complexes. Implications for photosynthetic water oxidation. J. Inorg. Biochem. 100, 1234-1243
105. Gonzalez, A., and Nave, C. (1994) Radiation damage in protein crystals at low temperature. Acta Crystallogr. D Biol. Crystallogr. 50, 874-877
106. Macedo, S., Pechlaner, M., Schmid, W., Weik, M., Sato, K., Dennison, C., and Djinović-Carugo, K. (2009) Can soaked-in scavengers protect metalloprotein active sites from reduction during data collection? J. Synchrotron Radiat. 16, 191-204
107. Umena, Y., Kawakami, K., Shen, J. R., and Kamiya, N. (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55-60
108. Schlichting, I., and Miao, J. (2012) Emerging opportunities in structural biology with x-ray free-electron lasers. Curr. Opin. Struct. Biol. 22, 613-626
109. Neutze, R., and Moffat, K. (2012) Time-resolved structural studies at synchrotrons and x-ray free electron lasers. Opportunities and challenges. Curr. Opin. Struct. Biol. 22, 651-659
110. Fromme, P., and Spence, J. C. (2011) Femtosecond nanocrystallography using x-ray lasers for membrane protein structure determination. Curr. Opin. Struct. Biol. 21, 509-516
111. Chapman, H. N., Fromme, P., Barty, A., White, T. A., Kirian, R. A., Aquila, A., Hunter, M. S., Schulz, J., DePonte, D. P., Weierstall, U., Doak, R. B., Maia, F. R., Martin, A. V., Schlichting, I., Lomb, L., Coppola, N., Shoeman, R. L., Epp, S. W., Hartmann, R., Rolles, D., Rudenko, A., Foucar, L., Kimmel, N., Weidenspointner, G., Holl, P., Liang, M., Barthelmess, M., Caleman, C., Boutet, S., Bogan, M. J., Krzywinski, J., Bostedt, C., Bajt, S., Gumprecht, L., Rudek, B., Erk, B., Schmidt, C., Hömke, A., Reich, C., Pietschner, D., Strüder, L., Hauser, G., Gorke, H., Ullrich, J., Herrmann, S., Schaller, G., Schopper, F., Soltau, H., Kühnel, K. U., Messerschmidt, M., Bozek, J. D., Hau-Riege, S. P., Frank, M., Hampton, C. Y., Sierra, R. G., Starodub, D., Williams, G. J., Hajdu, J., Timneanu, N., Seibert, M. M., Andreasson, J., Rocker, A., Jonsson, O., Svenda, M., Stern, S., Nass, K., Andritschke, R., Schroter, C. D., Krasniqi, F., Bott, M., Schmidt, K. E., Wang, X., Grotjohann, I., Holton, J. M., Barends, T. R., Neutze, R., Marchesini, S., Fromme, R., Schorb, S., Rupp, D., Adolph, M., Gorkhover, T., Andersson, I., Hirsemann, H., Potdevin, G., Graafsma, H., Nilsson, B., and Spence, J. C. (2011) Femtosecond x-ray protein nanocrystallography. Nature 470, 73-77
112. Kern, J., Alonso-Mori, R., Hellmich, J., Tran, R., Hattne, J., Laksmono, H., Glöckner, C., Echols, N., Sierra, R. G., Sellberg, J., Lassalle-Kaiser, B., Gildea, R. J., Glatzel, P., Grosse-Kunstleve, R. W., Latimer, M. J., Mc- Queen, T. A., DiFiore, D., Fry, A. R., Messerschmidt, M., Miahnahri, A., Schafer, D. W., Seibert, M. M., Sokaras, D., Weng, T. C., Zwart, P. H., White, W. E., Adams, P. D., Bogan, M. J., Boutet, S., Williams, G. J., Messinger, J., Sauter, N. K., Zouni, A., Bergmann, U., Yano, J., and Yachandra, V. K. (2012) Room temperature femtosecond x-ray diffraction of photosystem II microcrystals. Proc. Natl. Acad. Sci. U.S.A. 109, 9721-9726
113. Boutet, S., Lomb, L., Williams, G. J., Barends, T. R., Aquila, A., Doak, R. B., Weierstall, U., DePonte, D. P., Steinbrener, J., Shoeman, R. L., Messerschmidt, M., Barty, A., White, T. A., Kassemeyer, S., Kirian, R. A., Seibert, M. M., Montanez, P. A., Kenney, C., Herbst, R., Hart, P., Pines, J., Haller, G., Gruner, S. M., Philipp, H. T., Tate, M. W., Hromalik, M., Koerner, L. J., van Bakel, N., Morse, J., Ghonsalves, W., Arnlund, D., Bogan, M. J., Caleman, C., Fromme, R., Hampton, C. Y., Hunter, M. S., Johansson, L. C., Katona, G., Kupitz, C., Liang, M., Martin, A. V., Nass, K., Redecke, L., Stellato, F., Timneanu, N., Wang, D., Zatsepin, N. A., Schafer, D., Defever, J., Neutze, R., Fromme, P., Spence, J. C., Chapman, H. N., and Schlichting, I. (2012) High-resolution protein structure determination by serial femtosecond crystallography. Science 337, 362-364
114. Danford, J. J., Dobrowolski, P., and Berreau, L. M. (2009) Thioester hydrolysis reactivity of an Fe(III)Zn(II) complex. Inorg. Chem. 48, 11352-11361
115. Lomoth, R., Huang, P., Zheng, J., Sun, L., Hammarström, L., Akermark, B., and Styring, S. (2002) Synthesis and characterization of a dinuclear manganese(III,III) complex with three phenolate ligands. Eur. J. Inorg. Chem. 2002, 2965-2974